Lung Cancer Screening with Low-Dose Computed Tomography

Letters

RESEARCH LETTER to 80 years who have a 30 pack or more per year smoking history and currently smoke or have quit within the Lung Cancer Screening With past 15 years.2 According to the 2010 National Health Inter- Low-Dose Computed Tomography view Survey (NHIS), only 2% to 4% of high-risk smokers in the United States—2010 to 2015 received LDCT for lung cancer screening in the pre- Lung cancer is the most preventable and leading cause of vious year.3 In this study, we examined whether cancer deaths in the United States, with about 155 870 LDCT screening has increased following the USPSTF recom- deaths each year.1 In December 2013, the United States mendation. Preventive Services Task Force (USPSTF) recommended annual screening for lung cancer with low-dose computed Methods | We used the 2010 and 2015 NHIS, which included tomography (LDCT) for asymptomatic persons aged 55 2347 respondents who met the USPSTF criteria for LDCT.2 Self-

Table 1. Prevalence of LDCT Testing for Lung Cancer in the Past Year Among Screening-Eligible and Noneligible Smokers, National Health Interview Surveys 2010 and 2015a,b

Total 2010 2015 Characteristic No. (%) (95% CI) No. (%) (95% CI) No. (%) (95% CI) P Valuec Screening-eligible smokers (n = 2167) Weighted No. receiving LDCTd 276 700 262 700 Weighted No. eligible for LDCT 8 456 800 6 819 500 Total 2167 (3.5) (2.6-4.8) 1036 (3.3) (2.3-4.7) 1131 (3.9) (2.4-6.2) .60 Smoking history Former, ≥30 PY, quit ≤15 years 1020 (4.2) (2.7-6.5) 491 (4.0) (2.6-6.1) 529 (4.6)e (2.1-9.4)e .76 ago Current, ≥30 PY 1147 (2.9) (1.8-4.5) 545 (2.6)e (1.4-4.9)e 602 (3.2) (1.8-5.6) .64 Age, y 55-64 1119 (2.3) (1.5-3.6) 554 (2.8)e (1.6-5.1)e 565 (1.7) (1.0-3.1) .29 65-80 1048 (5.0) (3.3-7.6) 482 (3.8) (2.4-6.0) 566 (6.6)e (3.6-11.9)e .19 Sex Male 1245 (3.8) (2.6-5.4) 597 (3.8) (2.5-5.9) 648 (3.8) (2.2-6.3) .96 Female 922 (3.2)e (1.7-5.7)e 439 (2.5)e (1.2-5.0)e 483 (4.0)e (1.6-9.5)e .46 BMI <25 688 (5.6) (3.4-9.3) 320 (4.4)e (2.4-8.0)e 368 (7.2)e (3.3-14.7)e .36 ≥25 1400 (2.6) (1.8-3.7) 673 (2.7) (1.7-4.3) 727 (2.5) (1.5-4.2) .84 Usual place for medical care Yes 1965 (3.9) (2.9-5.3) 934 (3.6) (2.5-5.2) 1031 (4.3) (2.6-6.9) .60 No 202 (0.2)e (0.0-1.2)e 102e,f 100 (0.4)e (0.1-2.6)ef Visited PCP in past year Yes 1726 (4.3) (3.1-5.9) 813 (4.1) (2.9-5.9) 913 (4.5) (2.7-7.4) .78 No 440 (0.6) (0.2-1.8) 223f 217 (1.4) (0.5-4.1) f Insurance type Uninsured or Medicaid 1230 (4.2) (2.8-6.3) 586 (3.2) (2.0-5.1) 644 (5.5)e (3.0-9.9)e .20 Medicare, private, or other 937 (2.8) (1.7-4.4) 450 (3.4) (1.9-6.1) 487 (2.0)e (1.1-3.6)e .20 Raceg White 1787 (3.5) (2.5-5.0) 833 (3.1) (2.0-4.6) 954 (4.1) (2.4-6.9) .39 Nonwhite 380 (3.5) (2.0-6.2) 203 (4.7)e (2.3-9.5)e 177 (2.1)e (1.0-4.6)e .18 Education level

(continued)

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reported LDCT in the past year for lung cancer screening was mained low and constant, from 3.3% in 2010 to 3.9% in 2015 the primary outcome of the study. Analyses excluded respon- (P = .60); an even lower proportion of noneligible smokers re- dents with unknown (n = 6) or self-reported history of lung can- ceived LDCT (Table 1). Of the 6.8 million smokers eligible for cer (n = 41) or were missing LDCT testing information (n = 133), LDCT screening in 2015, only 262 700 received it. Further- leaving 2167 adults available for analyses. Weighted preva- more, there was no significant increase in screening from 2010 lence of LDCT for lung cancer screening in the past year was to 2015 for any of the sociodemographic groups, nor were there calculated by factors of interest. Multivariable prevalence ra- significant subgroup differences in screening, except be- tios of LDCT in the past year were estimated using predicted tween participants with or without a history of bronchitis margins. All statistical analyses accounted for complex sam- (Table 2). Of note, over 50% (1230/2167) of smokers meeting pling design and were conducted with SAS callable SUDAAN USPSTF recommendations for LDCT screening were unin- statistical software (version 9.0.3, SAS Institute). The study was sured or Medicaid insured (Table 1). based on deidentified publicly available database and ex- empt from institutional review board and informed consent. Discussion | Screening for lung cancer using LDCT among eligible current and former smokers remained low and un- Results | From 2010 to 2015, the percentage of eligible smok- changed in 2015 following the 2013 USPSTF recommenda- ers who reported LCDT screening in the past 12 months re- tion for annual screening. Reasons for exceptionally low uptake

Table 1. Prevalence of LDCT Testing for Lung Cancer in the Past Year Among Screening-Eligible and Noneligible Smokers, National Health Interview Surveys 2010 and 2015a,b (continued)

Total 2010 2015 Characteristic No. (%) (95% CI) No. (%) (95% CI) No. (%) (95% CI) P Valuec Income, $ <35 000 1130 (3.9) (2.8-5.3) 543 (3.9) (2.5-6.1) 587 (3.8) (2.3-6.2) .97 ≥35 000 926 (3.3) (2.0-5.4) 446 (2.8) (1.5-5.0) 480 (3.9)e (1.8-8.1)e .51 Family history of lung cancer Yes 362 (4.5)e (2.4-8.2)e 161 (4.8)e (2.0-10.8)e 201 (4.1)e (2.1-8.0)e .76 No 1709 (3.3) (2.3-4.8) 812 (2.8) (1.9-4.4) 897 (3.9) (2.1-6.9) .42 Attempted to quit smoking in the past 12 monthsh Yes 363 (4.1)e (2.1-8.0)e 164 (3.3)e (1.2-8.8)e 199 (5.1)e (2.1-12.3)e .52 No 784 (2.3) (1.3-3.9) 381 (2.3)e (1.0-5.2)e 403 (2.2)e (1.1-4.3)e .93 Ever diagnosed with emphysema Yes 321 (8.9) (5.8-13.4) 169 (9.6) (5.8-15.5) 152 (7.9)e (3.8-15.8)e .64 No 1844 (2.6) (1.7-3.9) 866 (2.0) (1.2-3.4) 978 (3.2)e (1.7-5.9)e .30 Ever diagnosed with bronchitis Yes 272 (11.2) (6.4-18.8) 135 (11.5) (6.5-19.7) 137 (10.7)e (3.6-27.7)e .90 No 1895 (2.4) (1.7-3.5) 901 (2.1) (1.3-3.3) 994 (2.9) (1.8-4.6) .30 Ever diagnosed with asthma Yes 327 (6.2) (3.7-10.1) 184 (8.0) (4.4-14.0) 143 (3.2)e (1.3-7.3)e .08 No 1838 (3.1) (2.1-4.5) 851 (2.3) (1.5-3.7) 987 (4.0) (2.3-6.7) .16 Noneligible smokers (n = 6632)i Total 6632 (2.4) (1.9-2.9) 2632 (2.0) (1.5-2.9) 3989 (2.7) (2.1-3.6) .12 Former, <30 PY, quit ≤15 years 932 (2.3) (1.3-4.1) 378 (3.1) (1.5-6.3) 554 (1.7) (0.7-4.4) .36 ago Former, ≥30 PY, quit >15 years 740 (4.0) (2.5-6.2) 339 (2.5) (1.1-5.4) 401 (5.8) (2.9-11.3) .17 ago Former, <30 PY, quit ≥15 years 3334 (1.6) (1.2-2.3) 1255 (1.5) (0.9-2.5) 2079 (1.7) (1.2-2.6) .68 ago Current, <30 PY 1626 (3.3) (2.3-4.6) 671 (2.0) (1.2-3.5) 955 (4.4) (2.8-6.6) .04 Abbreviations: BMI, body mass index (calculated as weight in kilograms divided d Weighted numbers take into account the assigned sampling weights of by height in meters squared); LDCT, low-dose computerized tomography; PCP, respondents. primary care physician; PY, pack-years. e Unreliable estimates as a result of relative standard errors exceeding 30%. a The following number of respondents were missing data for these items and f Unable to generate estimate owing to small denominator. are shown in parentheses: income (111), BMI (79), PCP visits (1), education (5), g White includes non-Hispanic whites, nonwhite includes: Hispanic, Asian, immigration status (1), family history of lung cancer (96), emphysema (2), Black, Native American/Alaskan Native and other race and/or ethnicities. asthma (2). Respondents with missing information were included in the model, but data are not shown. h Among current smokers only. b Percentages are weighted. i Includes former and current smokers who do not meet the US Preventive Services Task Force Recommendations. c P value compares 2010 vs 2015.

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of screening may include gaps in smokers’ knowledge regard- Table 2. Adjusted Prevalence Ratios and 95% CIs of LDCT Testing for Lung Cancer in the Past Year Among Screening-Eligible Respondents, ing LDCT, lack of access to care as well as physicians’ knowl- National Health Interview Survey 2010 and 2015 (n = 2167)a,b edge about screening recommendations4 and reimbursement. For example, according to a 2015 survey of physicians Characteristic PR (95% CI) in South Carolina, 36% of physicians correctly stated that LCDT Year screening should be conducted annually in high-risk individu- 2010 1 [Reference] als, and 63% of physicians did not know that Medicare covers 2015 1.28 (0.66-2.47) LDCT for lung cancer screening.4 It is also possible that phy- Age, y sicians may be aware of LDCT screening, but have limited ac- 55-64 1 [Reference] cess to the high-volume, and high-quality radiology centers, 65-80 1.34 (0.62-2.88) a recommendation set forth by public health organizations5 Sex and a stipulation on Medicare reimbursement.6 The decrease Male 1 [Reference] in the number of screening-eligible smokers from 8.4 million Female 0.61 (0.26-1.4) in 2010 to 6.8 million in 2015 reflects progress in tobacco con- BMI trol, and this has implications for the future provision of LDCT <25 1 [Reference] screening. Receipt of LDCT and smoking history were self- ≥25 0.36 (0.16-0.8) reported and subject to recall bias and the limited time fol- Usual place for medical care lowing the USPSTF recommendation and Medicare- Yes 1 [Reference] reimbursement are limitations of our study. Despite this, our No 0.12 (0.01-1.78) study provides the first national estimate of LDCT following Insurance type the USPSTF recommendation. Uninsured or medicaid 1 [Reference] In conclusion, annual LCDT screening among heavy Medicare, private, or other 0.94 (0.43-2.06) current and former smokers remains low and unchanged Racec following the USPSTF recommendation despite the poten- White 1 [Reference] tial to avert thousands of lung cancer deaths each year. This Nonwhite 1.31 (0.51-3.33) underscores the need to educate clinicians and smokers Education level about the benefit and risks of lung cancer screening for

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4. Ersek JL, Eberth JM, McDonnell KK, et al. Knowledge of, attitudes toward, screening in 2016 were eligible. Patients who could not and use of low-dose computed tomography for lung cancer screening among understand telephone or SMS, or did not have mobile phones family physicians. Cancer. 2016;122(15):2324-2331. were excluded. Participants were randomized by a computer- 5. Wender R, Fontham ET, Barrera E Jr, et al. American Cancer Society lung generated sequence with an allocation ratio of 1:1:1. In the cancer screening guidelines. CA Cancer J Clin. 2013;63(2):107-117. control group, participants were told in 2015 that they should 6. Centers for Medicare and Medicaid Services. Decision Memo for Screening for Lung Cancer with Low Dose Computed Tomography (LDCT) (CAG-00439N). visit the screening center for annual FIT pickup at the same 2015; https://www.cms.gov/medicare-coverage-database/details/nca-decision calendar month of 2016. In the SMS group, subjects received -memo.aspx?NCAId=274. Accessed January 13, 2017. a 1-way SMS, highlighting importance of CRC screening, and notifying date and location of FIT pickup on their mobile. In the telephone group, participants received a call from a trained Association of Interactive Reminders health care physician with the same message as the SMS, but and Automated Messages an interactive conversation was permitted. The interventions With Persistent Adherence to Colorectal were delivered 1 month before the expected date of participant Cancer Screening: A Randomized Clinical Trial return for second round of screening. The Joint Chinese The US Preventive Services Task Force recommends annual fe- University of Hong Kong–New Territories East Cluster Clinical cal immunochemical test (FIT) as one of the colorectal cancer Research Ethics Committee approved the study and participant (CRC) screening tests.1 Adherence to yearly FIT is crucial to pro- consent was waived because the interventions were an grammatic success.2 However, longitudinal adherence is low extension of the screening services. The trial protocol is and strategies to improve provided in the Supplement. Outcomes were rate of FIT pickup within 1 month of a pa- Supplemental content persistent adherence are needed.3 We evaluated the ef- tient’s anticipated return, and rate of FIT return within 2 months fectiveness of interactive telephone calls vs automated short of anticipated return. Six hundred patients provide 80% power message service (SMS) on improving adherence to FIT screen- (at 5% α level) for detecting an 11% increase in FIT return rate in ing compared with usual care. the intervention groups compared with control, which was as- sumed to have a FIT return rate of 70%.5 Associations between Methods | We conducted a prospective randomized parallel study groups and outcomes were examined by backward step- group study, with the setting previously described.4 The wise, binary logistic regression. Subgroup analysis for sex, mari- trial was registered on Clinicaltrials.gov (NCT02815436). tal status, household income, and educational level were per- Asymptomatic patients with negative FIT results in their first formed, because these factors were previously found to be screening round from April to September 2015 due for annual associated with screening adherence.6

Figure. Consort Flow Diagram

630 Assessed for eligibility

1 Excluded No mobile phone

629 Randomized

210 Allocated to control group 212 Allocated to SMS messages 207 Allocated to interactive telephone intervention messages intervention

78 Excluded 45 Excluded 21 Excluded Did not pick up FIT on time at Did not pick up FIT on time at Did not pick up FIT on time at follow-up follow-up follow-up

2 Excluded 3 Excluded 3 Excluded 1 Received colonoscopy in other Received colonoscopy in other Received colonoscopy in other sectors before second round of FIT sectors before second round of FIT sectors before second round of FIT 1 Change in bowel habits before second round of FIT

3 Excluded 3 Excluded 2 Excluded Already received cancer screening or Already received cancer screening or Already received cancer screening or not expected to return for follow-up not expected to return for follow-up not expected to return for follow-up

207 Analyzed 209 Analyzed 205 Analyzed FIT indicates fecal immunochemical test.

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